Preparing for future waves and pandemics: a global hospital survey on infection control measures and infection rates in COVID-19

A survey of hospitals on three continents was performed to assess their infection control preparedness and measures, and their infection rate in hospital health care workers during the COVID-19 pandemic. All surveyed hospitals used similar PPE but differences in preparedness, PPE shortages, and infection rates were reported.


Introduction
In the COVID-19 pandemic, the need for personal protective equipment (PPE) strongly increased to protect health care workers (HCWs) within the hospital from infection by COVID-19-positive patients [1]. Although our understanding of the novel coronavirus strain SARS-CoV-2 has been rapidly evolving, a detailed understanding on the modes of transmission is still lacking [2,3]. To protect HCWs, the World Health Organization and the Centers for Disease Control recommend the use of face masks, eye protection, gowns, medical gloves, frequent hand hygiene, environmental cleaning, and waste management [4]. The most potent protection, respirators which filter out at least 94% (FFP2, N95) or 99% (FFP3, N99) of airborne particles, as well as other PPE were quickly in short demand as the pandemic swept around the planet, resulting in shortages in many hospitals with a potential increase in COVID-19 infection risk for HCWs [5,6].
Our hypothesis was that the preparedness and response to the pandemic was different among hospitals, countries, and regions, and resulted in different exposure risk for HCWs in terms of COVID-19 prevalence and PPE availability. The goal of our study was to compare and assess the preparedness, the response, and the infection rate among hospital HCWs of several institutions on three continents by questionnaire.

Methods
No Institutional Review Board approval or informed patient consent was needed for this survey. The survey was performed between June and August 2020 at eight different institutions: Salzburg (Austria), Wuhan (China), Mannheim (Germany), Bergamo (Italy), Singapore, Hirslanden Klinik in Lucerne (Switzerland), an anonymized institution in the UK, Boston (MA, USA). Sites were recruited by emailing the Division of Infectious Diseases of each hospital. Surveys were sent out by email and reports were received by email.

Baseline characteristics of the surveyed hospitals and COVID-19 infection rates
The overall survey response rate was 100%. No incomplete survey responses were received.
Baseline characteristics of the eight hospitals included in the survey and the COVID-19 case load of their country are shown in Table 1 and Additional file 1: Table S1. Five hospitals are located in Europe (Austria, Germany, Italy, Switzerland, United Kingdom), two in Asia (China, Singapore) and one in North America (United States) (Additional file 1: Fig. S1).
All surveyed hospitals are mid-sized to large tertiary referral centers. The percentage of COVID-19-positive HCWs varied widely from 0.1 to 8.5%. The two Asian institutions showed low infection rates (≤ 1%) despite treating large numbers of COVID-19 positive patients.

Pandemic preparedness before the COVID-19 outbreak
All hospitals except two (Italy and United Kingdom) reported respiratory infectious disease outbreak preparedness with basic infection control trainings of any kind before the onset of the COVID-19 pandemic (Additional file 1: Table S2).
The institutions in China and Singapore noted that their plan for a pandemic with a respiratory infection was mainly based on the experience from the first SARS epidemic and the resulting policies. While the institution in Italy did not specifically prepare for a pandemic with a respiratory infectious disease, there was a course to prepare for an Ebola outbreak aimed at the Emergency Department in 2019. Furthermore, there was an emergency preparation meeting before the first COVID-19 patient was admitted to the Italian institution.

Personal protective equipment during the COVID-19 outbreak in case of close contact with COVID-19 patients
All surveyed hospitals reported the use of surgical masks or respirators (FFP2/3, N95) and other disposable PPE such as gloves, gowns, and hand disinfectants ( Table 2). Disposable caps and goggles were not used in two European hospitals. Other PPE used include face shields, visors, aprons, and air-purifying respirators in aerosolizing procedures. HCWs were trained to put on and use the PPE in all institutions.
Four of the eight surveyed institutions reported shortages in PPE at some point in the pandemic (Additional file 1: Table S3). Masks or respirators were missing for at least a brief period of time at the institutions in Austria, Germany, Italy, and the US. Three of the eight institutions  10:170 reported that disposable gowns were not available during the entire time of the pandemic. Single institutions further reported shortages in gloves and disinfectants, and the need for rationing PPE to avoid shortages.

Management of the pandemic
Infectious disease specialists were in charge of the management of the pandemic in all surveyed hospitals except for the one in the UK where non-specialized physicians were responsible (Additional file 1: Table S4). All hospitals put a task force in charge of coordinating the safety measures to reduce viral spread in the hospital, and implemented zoning (i.e., areas designated for suspected and confirmed COVID-19 patients), grouping COVID-19-positive patients (cohorting), hygiene trainings, and restrictions for visitors. Masking of HCWs in the entire hospital was mandated by all hospitals except for the one in Salzburg, where it was recommended. Visitor restrictions were put in place in all surveyed hospitals, with two hospitals allowing no visitors and two only allowing compassionate visits.

Discussion
In this study, we evaluated the preparedness, the management, and the infection rate of hospital HCWs of the COVID-19 pandemic of eight hospitals located in Europe, Asia, and North America. While most hospitals were prepared for a pandemic with a respiratory disease, there were shortages in several PPE, namely masks and gowns. The percentage of COVID-19-positive hospital workers ranged from 0.1 to 8.5%. Notably, the Asian hospitals reported no shortages in surgical masks or respirators and showed low infection rates (≤ 1%) despite high numbers of treated COVID-19 patients. Without pointing fingers, this survey helps us identify key aspects of preparedness in terms of planification and PPE item stockage, in order to be better prepared for future waves of COVID-19 and other pandemics with respiratory viruses. The low infection numbers despite high caseloads in Asian hospital may be explained by the experience with the SARS epidemic in 2002/2003 which mainly affected Asian countries such as China, Singapore, Vietnam, and Hong Kong. Hospital transmission accounted for a 22 to 57% of SARS cases [7], and was primarily related to inappropriate or missing PPE, hand disinfection, and hospital personnel education (e.g., removal of contaminated PPE) [8]. As a result, these countries prepared sophisticated plans to manage future pandemics, mandating training hospital personnel for pandemics with respiratory pathogens, stockpiling PPE, and further measures such as zoning [9]. As no shortages in masks and respirators were reported by these hospitals, their stockpiling has likely contributed to the low infection rates in these hospitals, which underlines their importance in protecting HCWs from COVID-19 patients. In our survey, countries with less exposure to the first SARS epidemic, namely in Europe and the US, were less prepared in terms of personnel training and/or PPE stockpiling, and experienced more PPE shortages and higher numbers of infected hospital HCWs. However, hospitals showed a steep learning curve, adopting measures such as universal masking for hospital personnel and proving their usefulness for infection control [10][11][12].
As we prepare for the next waves of COVID-19, we have learned that universal masking of hospital personnel with surgical masks, immediately isolating COVID-19-positive patients, and the use of highly protective PPE (respirators, eye protection, gowns) in contact with COVID-19 patients is of high utility to protect HCWs [4,13]. As some of these insights were already available after the SARS epidemic and improved the response of the surveyed Asian hospitals to the COVID-19 pandemic, it is instrumental for hospitals to learn from each other's experiences and to cooperate to improve hospital infection control in future waves of COVID-19 and other pandemics. Based on the information of this survey, it will be essential to either stock higher amounts of PPE or to have the capacity to produce or recycle PPE locally to be prepared for future disruptions in supply chains.
This study has several limitations. Most importantly, we cannot determine if the COVID-19 positive hospital HCWs were infected in the hospital or outside. Indeed, the true extent of COVID-19 is difficult to assess [14,15]. Another limitation of the study is that the questionnaire was filled out when some countries were still in the first wave while others were past the first wave (e.g., China). Furthermore, there might be a selection bias as most hospitals were selected based on previous collaborations. Another limitation is that all surveyed hospitals are located in upper-middle to high-income countries. Finally, some surveyed European hospitals treated low numbers of COVID-19 patients, complicating the evaluation of their true preparedness.
In this survey, all responding hospitals in Asia, Europe, and North America reported the use of recommended PPE but the degree of preparedness, PPE shortages, and infection rate among hospital HCWs varied widely. Our study highlights the importance of universal masking of HCWs with surgical masks, immediately isolating COVID-19-positive patients, and the use of highly protective PPE (respirators, eye protection, gowns). To prepare for the next waves of COVID-19 and future pandemics, we further urge hospitals to learn from each other and to cooperate to improve infection control.
Additional file 1: Supplementary Figure and Tables.